Superior colliculus lesions in rat abolish exploratory head-dipping in hole-board test

Dean, Paul; Pope, Sian G.; Redgrave, Peter; Donohoe, Thomas P.

doi:10.1016/0006-8993(80)91149-x

Cited by 39 publications

(8 citation statements)

References 13 publications

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“…Orienting to experimenter-produced vibrissal stimulation is severely impaired by collicular lesions [52], [53], [54], as is orienting to novel environmental features encountered by the vibrissa during free movement in an open field [54], [55]. In addition, direct or indirect activation of the superior colliculus can result in enhanced orienting and biting to vibrissal stimulation [56], [57], and in what appears to be a type of ‘ghost’ orienting in the form of persistent circling and gnawing [58].…”

Section: Resultsmentioning

confidence: 99%

An Internal Model Architecture for Novelty Detection: Implications for Cerebellar and Collicular Roles in Sensory Processing

et al. 2012

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The cerebellum is thought to implement internal models for sensory prediction, but details of the underlying circuitry are currently obscure. We therefore investigated a specific example of internal-model based sensory prediction, namely detection of whisker contacts during whisking. Inputs from the vibrissae in rats can be affected by signals generated by whisker movement, a phenomenon also observable in whisking robots. Robot novelty-detection can be improved by adaptive noise-cancellation, in which an adaptive filter learns a forward model of the whisker plant that allows the sensory effects of whisking to be predicted and thus subtracted from the noisy sensory input. However, the forward model only uses information from an efference copy of the whisking commands. Here we show that the addition of sensory information from the whiskers allows the adaptive filter to learn a more complex internal model that performs more robustly than the forward model, particularly when the whisking-induced interference has a periodic structure. We then propose a neural equivalent of the circuitry required for adaptive novelty-detection in the robot, in which the role of the adaptive filter is carried out by the cerebellum, with the comparison of its output (an estimate of the self-induced interference) and the original vibrissal signal occurring in the superior colliculus, a structure noted for its central role in novelty detection. This proposal makes a specific prediction concerning the whisker-related functions of a region in cerebellar cortical zone A2 that in rats receives climbing fibre input from the superior colliculus (via the inferior olive). This region has not been observed in non-whisking animals such as cats and primates, and its functional role in vibrissal processing has hitherto remained mysterious. Further investigation of this system may throw light on how cerebellar-based internal models could be used in broader sensory, motor and cognitive contexts.

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Section: Resultsmentioning

confidence: 99%

An Internal Model Architecture for Novelty Detection: Implications for Cerebellar and Collicular Roles in Sensory Processing

et al. 2012

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“…Collicular animals usually run faster than normals in runways Murison & Mayes 1980), which perhaps causes them to make premature, ballistic "approach errors" to incorrect discriminanda (Schneider 1969;Winterkorn 1975), especially when discriminanda are unexpectedly changed (Thinus- Blanc 1983). They are hyperactive in a head-dip apparatus (Dean, Pope, Redgrave & Donohoe 1980;Foreman 1983a), on initial placement in open arenas (Dean, Pope & Redgrave 1982;Marshall 1978;Pope & Dean 1979), in operant chambers (Capps & Stockwell, 1968), and in spatial mazes, when test intervals are as short as 2 minutes (Smith & Weldon 1976). They also swim faster than controls (Milner & Lines 1983).…”

Section: Motor Control and Behavioural Inhibition I Open Field Hypermentioning

confidence: 99%

“…However, collicular animals do not collide with stationary objects; indeed, they negotiate barriers and obstacles well (Casagrande & Diamond 1974;Marshall 1978), implying that they are aware of the presence of such objects. Yet when placed in a novel arena, they typically remain close to the perimeter and do neglect holes in the apparatus floor, often falling into them (Dean et al 1980;Foreman 1983a). A striking parallel is evident in the hippocampal literature: O'Keefe and Nadel (1978) argue that hippocampal animals are "hyperactive but hypoexploratory."…”

Section: Motor Control and Behavioural Inhibition II Activity And Atmentioning

confidence: 99%

Relationships between the superior colliculus and hippocampus: Neural and behavioral considerations

Foreman

Stevens

1987

Behav Brain Sci

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Theories of superior collicular and hippocampal function have remarkable similarities. Both structures have been repeatedly implicated in spatial and attentional behaviour and in inhibitory control of locomotion. Moreover, they share certain electrophysiological properties in their single unit responses and in the synchronous appearance and disappearance of slow wave activity. Both are phylogenetically old and the colliculus projects strongly to brainstem nuclei instrumental in the generation of theta rhythm in the hippocampal EECOn the other hand, close inspection of behavioural and electrophysiological data reveals disparities. In particular, hippocampal processing mainly concerns stimulus ambiguity, contextual significance, and spatial relations or other subtle, higher order characteristics. This requires the use of largely preprocessed sensory information and mediation of poststimulus investigation. Although collicular activity must also be integrated with that of “higher” centres (probably to a varying degree, depending on the nature of stimuli being processed and the task requirements), its primary role in attention is more “peripheral” and specific in controlling orienting/localisation via eye and body movements toward egocentrically labelled spatial positions. In addition, the colliculus may exert a nonspecific influence in alerting higher centres to the imminence of information potentially worthy of focal attention. Nevertheless, it is noteworthy that collicular and hippocampal lesions produce deficits on similar tasks, although the type of deficit is usually different (often opposite) in each case. Functional overlap between hippocampus and colliculus (i.e., strategically synchronised or mutually interdependent activity) is virtually certain vis-à-vis stimulus sampling, for example in the acquisition of information via vibrissal movements and visual scanning. In addition, insofar as stimulus significance is a factor in collicular orienting mechanisms, the hippocampus — cingulate – cortex — colliculus pathway may play a significant role, modulating collicular responsiveness and thus ensuring an attentional strategy appropriate to current requirements (stimulus familiarity, stage of learning). A tentative “reciprocal loop” model is proposed which bridges physiological and behavioural levels of analysis and which would account for the observed degree and nature of functional overlap between the superior colliculus and hippocampus.

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“…Although locomotor activity is the usual measure of exploratory level (Berlyne, 1960), it would not allow a fine analysis of exploratory reactions toward spatially welldefined objects. Moreover, locomotor activity can be a misleading measure of exploratory behavior, since certain brain damage such as lesions of the superior collicuIus (Dean, Pope, Redgrave, & Donohoe, 1980) or of the septum (Ellen & Weston, 1983), induce hyperactivity in rats without the responses being typical of exploration or curiosity.…”

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A study of exploratory behavior as an index of spatial knowledge in hamsters

Poucet

Chapuis

Durup

et al. 1986

Animal Learning & Behavior

149

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This experiment investigated the role of exploration in the formation of maps of the environment. The effects of spatial rearrangement of four familiar objects in an open field on subsequent exploratory behavior were studied in hamsters (Mesocricetus auratus). During two exploratory sessions, four groups of subjects were exposed to objects in a particular spatial relation to each other and to a distal pattern. During a testing session, the control group was exposed to the same situation as during the first two sessions, and the three experimental groups were exposed to various object rearrangements. The hamsters in the experimental groups, but not those in the control group, renewed their exploration of the objects during the testing session, as measured by the number of contacts with the objects and the time spent investigating them. Further analyses of the nature ofthe reinvestigated objects (i.e., displaced or nondisplaced) support the hypothesis that, through exploration, a long-lasting representation of the environment is built up on the basis of the topological relations among the objects, the overall geometric structure provided by the arrangement of the objects, and the relations between the objects and extra-apparatus landmarks.Following the pioneer studies by Hall (1934), who used the open field to test the effects of unfamiliar environments upon emotionality in rats, many experiments have been concerned with the intensity of exploratory reactions to new stimuli such as congeneric scents and illumination level and environmental complexity (e.g., Schenk, 1979), as well as water, food, or new objects introduced into a familiar environment (e.g., Cowan, 1976). In contrast to the number of experiments focusing upon the effect of the characteristics of new objects on the amount of exploration, few studies have attempted to provide evidence that exploratory reactions are also induced by new spatial arrangements of familiar objects. In one experiment, Wilz and Bolton (1971) allowed gerbils to explore an open field that contained either only one object, or a group of objects in fixed locations. After habituation (i.e., extinction of exploration), a new arrangement of the objects or a change in the location of the single object elicited a renewal of exploration as intense as a totally new situation would have done. Similar results were obtained in other experiments with gerbils (Cheal, 1978; ThinusBlanc & Ingle, 1985) and rats (Corman, Meyer, & Meyer, 1967;Corman & Shafer, 1968;Dember, 1956;Lukaszewska, 1978;Lukaszewska & Dlawichowska, 1982). Such data strongly suggest that exploratory be- 93havior involves the gathering of information not only about the qualities of the objects but also about their spatial relationships.Indirect evidence of this function of exploration is provided by the results obtained in spatial problem solving tests. Maier (1932) and, more recently, Stahl and Ellen (1974), Herrmann, Bahr, Bremner, and, and Ellen, Parko, Wages, Doherty, and Herrmann (1982) showed that rats need an exte...

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Superior colliculus lesions in rat abolish exploratory head-dipping in hole-board test

Cited by 39 publications

References 13 publications

An Internal Model Architecture for Novelty Detection: Implications for Cerebellar and Collicular Roles in Sensory Processing

An Internal Model Architecture for Novelty Detection: Implications for Cerebellar and Collicular Roles in Sensory Processing

Relationships between the superior colliculus and hippocampus: Neural and behavioral considerations

A study of exploratory behavior as an index of spatial knowledge in hamsters

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